Lifetime Reproductive Success and Heritability in Nature

The observation that traits closely related to fitness (“fitness traits”) have lower heritabilities than traits more distantly associated with fitness has traditionally been framed in terms of Fisher’s fundamental theorem of natural selection—fitness traits are expected to have low levels of additive genetic variance due to rapid fixation of alleles conferring highest fitness. Subsequent treatments have challenged this view by pointing out that high environmental and nonadditive genetic contributions to phenotypic variation may also explain the low heritability of fitness traits. Analysis of a large data set from the collared flycatcher Ficedula albicollis confirmed a previous finding that traits closely associated with fitness tend to have lower heritability. However, analysis of coefficients of additive genetic variation (CVA) revealed that traits closely associated with fitness had higher levels of additive genetic variation (VA) than traits more distantly associated with fitness. Hence, the negative relationship between a trait’s association with fitness and its heritability was not due to lower levels of VA in fitness traits but was due to their higher residual variance. However, whether the high residual variance was mainly due to higher levels of environmental variance or due to higher levels of nonadditive genetic variance remains a challenge to be addressed by further studies. Our results are consistent with earlier suggestions that fitness‐related traits may have more complex genetic architecture than traits more distantly associated with fitness.

[1]  B. Sheldon,et al.  Patterns of natural selection on morphology of male and female collared flycatchers (Ficedula albicollis) , 2000 .

[2]  B. Sheldon,et al.  Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas , 1999, Heredity.

[3]  H. Ellegren,et al.  Sexual selection resulting from extrapair paternity in collared flycatchers , 1999, Animal Behaviour.

[4]  J. Potti MATERNAL EFFECTS AND THE PERVASIVE IMPACT OF NESTLING HISTORY ON EGG SIZE IN A PASSERINE BIRD , 1999, Evolution; international journal of organic evolution.

[5]  L. L. Wolf,et al.  REPRODUCTIVE CHARACTERISTICS OF THE FLOWER BREEDING DROSOPHILA HIBISCI BOCK (DROSOPHILIDAE) IN EASTERN AUSTRALIA: GENETIC AND ENVIRONMENTAL DETERMINANTS OF OVARIOLE NUMBER , 1998, Evolution; international journal of organic evolution.

[6]  H. Ellegren,et al.  QUANTITATIVE GENETICS OF SEXUAL SIZE DIMORPHISM IN THE COLLARED FLYCATCHER, FICEDULA ALBICOLLIS , 1998, Evolution; international journal of organic evolution.

[7]  Cai-guo Xu,et al.  Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. Campbell GENETIC AND ENVIRONMENTAL VARIATION IN LIFE‐HISTORY TRAITS OF A MONOCARPIC PERENNIAL: A DECADE‐LONG FIELD EXPERIMENT , 1997, Evolution; international journal of organic evolution.

[9]  L. Gustafsson,et al.  Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  L. Rowe,et al.  The lek paradox and the capture of genetic variance by condition dependent traits , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  M. Lynch,et al.  Comparing mutational variabilities. , 1996, Genetics.

[12]  D. Roff,et al.  Dominance variance: associations with selection and fitness , 1995, Heredity.

[13]  K. Hughes THE EVOLUTIONARY GENETICS OF MALE LIFE‐HISTORY CHARACTERS IN DROSOPHILA MELANOGASTER , 1995, Evolution; international journal of organic evolution.

[14]  L. Gustafsson,et al.  Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers , 1995, Nature.

[15]  Austin Burt,et al.  Perspective: The Evolution of Fitness , 1995 .

[16]  Austin Burt,et al.  THE EVOLUTION OF FITNESS , 1995, Evolution; international journal of organic evolution.

[17]  L. Gustafsson,et al.  Seasonal decline in collared flycatcher ficedula albicollis reproductive success: an experimental approach , 1994 .

[18]  L. Gustafsson,et al.  Foster parent experiment reveals no genotype-environment correlation in the external morphology of Ficedula albicollis, the collared flycatcher , 1994, Heredity.

[19]  F. Messina Heritability and ‘evolvability’ of fitness components in Callosobruchus maculatus , 1993, Heredity.

[20]  L. Gustafsson,et al.  Inheritance of size and shape in a natural population of collared flycatchers, Ficedula albicollis , 1993 .

[21]  D. Schluter,et al.  MATERNAL INHERITANCE OF CONDITION AND CLUTCH SIZE IN THE COLLARED FLYCATCHER , 1993, Evolution; international journal of organic evolution.

[22]  D. Stratton LIFE‐CYCLE COMPONENTS OF SELECTION IN ERIGERON ANNUUS: II. GENETIC VARIATION , 1992, Evolution; international journal of organic evolution.

[23]  D. Houle Comparing evolvability and variability of quantitative traits. , 1992, Genetics.

[24]  D. Schluter,et al.  ON THE LOW HERITABILITY OF LIFE‐HISTORY TRAITS , 1991, Evolution; international journal of organic evolution.

[25]  D. Houle GENETIC COVARIANCE OF FITNESS CORRELATES: WHAT GENETIC CORRELATIONS ARE MADE OF AND WHY IT MATTERS , 1991, Evolution; international journal of organic evolution.

[26]  D. Levin,et al.  QUANTITATIVE GENETICS OF FITNESS TRAITS IN A WILD POPULATION OF PHLOX , 1991, Evolution; international journal of organic evolution.

[27]  T. Pärt Philopatry and age as factors influencing reproductive success in the collared flycatcher (Ficedula albicollis) , 1991 .

[28]  M. Kirkpatrick,et al.  The evolution of mating preferences and the paradox of the lek , 1991, Nature.

[29]  J. Gentle,et al.  Randomization and Monte Carlo Methods in Biology. , 1990 .

[30]  L. Gustafsson,et al.  Acceleration of senescence in the collared flycatcher Ficedula albicollis by reproductive costs , 1990, Nature.

[31]  D. Wiggins Food availability, growth, and heritability of body size in nestling tree swallows (Tachycineta bicolor) , 1990 .

[32]  L. Gustafsson,et al.  BREEDING DISPERSAL IN THE COLLARED FLYCATCHER (FICEDULA ALBICOLLIS): POSSIBLE CAUSES AND REPRODUCTIVE CONSEQUENCES , 1989 .

[33]  N. Barton,et al.  Evolutionary quantitative genetics: how little do we know? , 1989, Annual review of genetics.

[34]  W. Sutherland,et al.  The costs of reproduction in the collared flycatcher Ficedula albicollis , 1988, Nature.

[35]  C. Cockerham,et al.  Variance components of fitness under stabilizing selection. , 1988, Genetical research.

[36]  Js Jones,et al.  The heritability of fitness: Bad news for 'good genes'? , 1987, Trends in ecology & evolution.

[37]  L. Gustafsson Lifetime Reproductive Success and Heritability: Empirical Support for Fisher's Fundamental Theorem , 1986, The American Naturalist.

[38]  B. Charlesworth,et al.  Genetics of life history in Drosophila melanogaster. I. Sib analysis of adult females. , 1981, Genetics.

[39]  James N. M. Smith,et al.  EXPERIMENTAL CONFIRMATION OF HERITABLE MORPHOLOGICAL VARIATION IN A NATURAL POPULATION OF SONG SPARROWS , 1980, Evolution; international journal of organic evolution.

[40]  J. Crow,et al.  The genetic variance for viability and its components in a local population of Drosophila melanogaster. , 1974, Genetics.

[41]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .

[42]  M. Kimura On the change of population fitness by natural selection2 3 , 1958, Heredity.

[43]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.